Spatiotemporal Dynamics of Bimanual Integration in Human Somatosensory Cortex and Their Relevance to Bimanual Object Manipulation

Abstract

Little is known about the spatiotemporal dynamics of cortical responses that integrate slightly asynchronous somatosensory inputs from both hands. This study aimed to clarify the timing and magnitude of interhemispheric interactions during early integration of bimanual somatosensory information in different somatosensory regions and their relevance for bimanual object manipulation and exploration. Using multi-fiber probabilistic diffusion tractography and MEG source analysis of conditioning-test (C-T) median nerve somatosensory evoked fields in healthy human subjects, we sought to extract measures of structural and effective callosal connectivity between different somatosensory cortical regions and correlated them with bimanual tactile task performance. Neuromagnetic responses were found in major somatosensory regions, i.e., primary somatosensory cortex SI, secondary somatosensory cortex SII, posterior parietal cortex, and premotor cortex. Contralateral to the test stimulus, SII activity was maximally suppressed by 51% at C-T intervals of 40 and 60 ms. This interhemispheric inhibition of the contralateral SII source activity correlated directly and topographically specifically with the fractional anisotropy of callosal fibers interconnecting SII. Thus, the putative pathway that mediated inhibitory interhemispheric interactions in SII was a transcallosal route from ipsilateral to contralateral SII. Moreover, interhemispheric inhibition of SII source activity correlated directly with bimanual tactile task performance. These findings were exclusive to SII. Our data suggest that early interhemispheric somatosensory integration primarily occurs in SII, is mediated by callosal fibers that interconnect homologous SII areas, and has behavioral importance for bimanual object manipulation and exploration.

Dynamic network structure of interhemispheric coordination

“…Dynamic causal modeling, for example, has been used to provide complementary insights into the role of transcallosal coupling (67) in related lateralization effects (68,69) by estimating the effective connectivity rather than the functional connectivity between regions of interest. Indeed, the choice of connectivity estimate is an open one (21), and different measures of association might provide additional information regarding transfers occurring in other frequency bands (70,71).…”

Distinct fine‐scale fMRI activation patterns of contra‐ and ipsilateral somatosensory areas 3b and 1 in humans

“…Extending previous findings, here we provide evidence supporting distinct functional organization of digit activations within bilateral S1 cortex (area 3b and area 1), indicating their different roles in processing or modulating unilateral tactile inputs. Although ipsilateral S1 activation has been linked to performing bimanual tasks or tactile learning that engage inter-hemispheric interaction (Harris et al 2001, Jung et al 2012), studies are necessary to establish the specific functional roles of ipsilateral area 3b and area 1 in touch perception. Our observation of non-stimulus (digit) selective and non-somatotopic response features of ipsilateral area 3b activation exclude its role in fine spatial tactile discrimination.…”

Inter-hemispheric functional connectivity changes with corpus callosum morphology in multiple sclerosis

“…Inter-hemispheric functional connectivity as expressed by an index of synchronization (IHCoh) between tonically firing corticospinal cells in homologous sensorimotor rolandic cortices was associated with a reduction of callosal thickness at the level of the anterior mid-body. These regions convey few connections between homologous primary sensorimotor areas (Hofer and Frahm, 2006; Zarei et al, 2006), as well as fibers from secondary motor and somatosensory hand regions (Jung et al, 2012). Their relevance in sensorimotor control is confirmed by a selective dependence on handedness in healthy people (Witelson, 1989; Stancak et al, 2000, 2002).…”

“…Their relevance in sensorimotor control is confirmed by a selective dependence on handedness in healthy people (Witelson, 1989; Stancak et al, 2000, 2002). Moreover, they are engaged during bimanual object manipulation and exploration (Jung et al, 2012). This supports the concept that CC structure variability reflects inter-individual differences in skilled performance (Johansen-Berg et al, 2007).…”